Abstract
In the current study we investigated the effect of repetitive transcranial magnetic stimulation (rTMS) at different frequencies on chemical kindling in rats. Chemical kindling was induced by injection of pentylenetetrazol (PTZ; 45 mg/kg) at the intervals of 48 h between the injections. In the first experiment, effect of 0.25, 1 and 5 Hz rTMS (four trains of 4 s at motor threshold intensity) on kindling acquisition was investigated. In the second experiment, the stability of rTMS effects was checked in animals of the first experiment during a follow-up period of 2 weeks. Animals received a single dose of PTZ at 7th and 14th day after the last PTZ injection (12th injection) and their seizure parameters were recorded. Obtained results showed that application of rTMS at the frequencies of 0.25 and 1 Hz had anticonvulsant effect and decreased the PTZ kindling acquisition. However, when applied at the frequency of 5 Hz, it had an increasing effect on PTZ kindling rate. During the follow-up study, the seizure severity increased in animals treated with 0.25 Hz rTMS (and somehow in animals treated with 1 Hz rTMS), but did not change in animals treated with 5 Hz rTMS compared to the 12th PTZ injection. Our results showed that rTMS application may have an anticonvulsant effect during chemical kindling acquisition at very low frequency (0.25 Hz) and can increase the seizure severity at high frequency (5 Hz). However, during follow-up, the anticonvulsant effects of rTMS may be converted to proconvulsive effects.
Similar content being viewed by others
References
Bae EH, Schrader LM, Machii K, Alonso-Alonso M, Riviello JJ Jr, Pascual-Leone A, Rotenberg A (2007) Safety and tolerability of repetitive transcranial magnetic stimulation in patients with epilepsy: a review of the literature. Epilepsy Behav 10:521–528
Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403
Wassermann EM, Lisanby SH (2001) Therapeutic application of repetitive transcranial magnetic stimulation: a review. Clin Neurophysiol 112:1367–1377
Cantello R, Rossi S, Varrasi C, Ulivelli M, Civardi C, Bartalini S, Vatti G, Cincotta M, Borgheresi A, Zaccara G, Quartarone A, Crupi D, Lagana A, Inghilleri M, Giallonardo AT, Berardelli A, Pacifici L, Ferreri F, Tombini M, Gilio F, Quarato P, Conte A, Manganotti P, Bongiovanni LG, Monaco F, Ferrante D, Rossini PM (2007) Slow repetitive TMS for drug-resistant epilepsy: clinical and EEG findings of a placebo-controlled trial. Epilepsia 48:366–374 (Epub 2007/02/14)
Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 133:425–430
Pascual-Leone A, Houser CM, Reese K, Shotland LI, Grafman J, Sato S, Valls-Sole J, Brasil-Neto JP, Wassermann EM, Cohen LG et al (1993) Safety of rapid-rate transcranial magnetic stimulation in normal volunteers. Electroencephalogr Clin Neurophysiol 89:120–130
Wassermann EM, Grafman J, Berry C, Hollnagel C, Wild K, Clark K, Hallett M (1996) Use and safety of a new repetitive transcranial magnetic stimulator. Electroencephalogr Clin Neurophysiol 101:412–417
Romero JR, Anschel D, Sparing R, Gangitano M, Pascual-Leone A (2002) Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex. Clin Neurophysiol 113:101–107
Pascual-Leone A, Tormos JM, Keenan J, Tarazona F, Canete C, Catala MD (1998) Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol 15:333–343
Fisher RS (1989) Animal models of the epilepsies. Brain Res Brain Res Rev 14:245–278
Akamatsu N, Fueta Y, Endo Y, Matsunaga K, Uozumi T, Tsuji S (2001) Decreased susceptibility to pentylenetetrazol-induced seizures after low-frequency transcranial magnetic stimulation in rats. Neurosci Lett 310:153–156
Jennum P, Klitgaard H (1996) Repetitive transcranial magnetic stimulations of the rat. Effect of acute and chronic stimulations on pentylenetetrazole-induced clonic seizures. Epilepsy Res 23:115–122
Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281–294
Cincotta M, Borgheresi A, Gambetti C, Balestrieri F, Rossi L, Zaccara G, Ulivelli M, Rossi S, Civardi C, Cantello R (2003) Suprathreshold 0.3 Hz repetitive TMS prolongs the cortical silent period: potential implications for therapeutic trials in epilepsy. Clin Neurophysiol 114:1827–1833
Steinhoff BJ, Stodieck SR, Zivcec Z, Schreiner R, von Maffei C, Plendl H, Paulus W (1993) Transcranial magnetic stimulation (TMS) of the brain in patients with mesiotemporal epileptic foci. Clin Electroencephalogr 24:1–5
Tergau F, Naumann U, Paulus W, Steinhoff BJ (1999) Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 353:2209
Menkes DL, Gruenthal M (2000) Slow-frequency repetitive transcranial magnetic stimulation in a patient with focal cortical dysplasia. Epilepsia 41:240–242
Theodore WH, Hunter K, Chen R, Vega-Bermudez F, Boroojerdi B, Reeves-Tyer P, Werhahn K, Kelley KR, Cohen L (2002) Transcranial magnetic stimulation for the treatment of seizures: a controlled study. Neurology 59:560–562
Anschel DJ, Pascual-Leone A, Holmes GL (2003) Anti-kindling effect of slow repetitive transcranial magnetic stimulation in rats. Neurosci Lett 351:9–12
Ebert U, Ziemann U (1999) Altered seizure susceptibility after high-frequency transcranial magnetic stimulation in rats. Neurosci Lett 273:155–158
Ogiue-Ikeda M, Kawato S, Ueno S (2003) The effect of repetitive transcranial magnetic stimulation on long-term potentiation in rat hippocampus depends on stimulus intensity. Brain Res 993:222–226
Misawa S, Kuwabara S, Shibuya K, Mamada K, Hattori T (2005) Low-frequency transcranial magnetic stimulation for epilepsia partialis continua due to cortical dysplasia. J Neurol Sci 234:37–39
Santiago-Rodriguez E, Cardenas-Morales L, Harmony T, Fernandez-Bouzas A, Porras-Kattz E, Hernandez A (2008) Repetitive transcranial magnetic stimulation decreases the number of seizures in patients with focal neocortical epilepsy. Seizure 17:677–683
Rotenberg A, Muller P, Birnbaum D, Harrington M, Riviello JJ, Pascual-Leone A, Jensen FE (2008) Seizure suppression by EEG-guided repetitive transcranial magnetic stimulation in the rat. Clin Neurophysiol 119:2697–2702
Berardelli A, Inghilleri M, Rothwell JC, Romeo S, Curra A, Gilio F, Modugno N, Manfredi M (1998) Facilitation of muscle evoked responses after repetitive cortical stimulation in man. Exp Brain Res 122:79–84
Lorenzano C, Gilio F, Inghilleri M, Conte A, Fofi L, Manfredi M, Berardelli A (2002) Spread of electrical activity at cortical level after repetitive magnetic stimulation in normal subjects. Exp Brain Res 147:186–192
Di Lazzaro V, Oliviero A, Mazzone P, Pilato F, Saturno E, Dileone M, Insola A, Tonali PA, Rothwell JC (2002) Short-term reduction of intracortical inhibition in the human motor cortex induced by repetitive transcranial magnetic stimulation. Exp Brain Res 147:108–113
Jennum P, Winkel H, Fuglsang-Frederiksen A (1995) Repetitive magnetic stimulation and motor evoked potentials. Electroencephalogr Clin Neurophysiol 97:96–101
Wu T, Sommer M, Tergau F, Paulus W (2000) Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett 287:37–40
Fitzgerald PB, Fountain S, Daskalakis ZJ (2006) A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol 117:2584–2596
Tassinari CA, Cincotta M, Zaccara G, Michelucci R (2003) Transcranial magnetic stimulation and epilepsy. Clin Neurophysiol 114:777–798
Weiss SR, Li XL, Rosen JB, Li H, Heynen T, Post RM (1995) Quenching: inhibition of development and expression of amygdala kindled seizures with low frequency stimulation. NeuroReport 6:2171–2176
Huang CC, Lee CC, Hsu KS (2004) An investigation into signal transduction mechanisms involved in insulin-induced long-term depression in the CA1 region of the hippocampus. J Neurochem 89:217–231
Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN, Rothwell JC (2004) Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24:3379–3385
Schubert M, Siegmund H, Pape HC, Albrecht D (2005) Kindling-induced changes in plasticity of the rat amygdala and hippocampus. Learn Mem 12:520–526
Acknowledgments
This study was granted by Research Chancellor of Tarbiat Modares University, Tehran, Iran.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mongabadi, S., Firoozabadi, S.M., Javan, M. et al. Effect of different frequencies of repetitive transcranial magnetic stimulation on acquisition of chemical kindled seizures in rats. Neurol Sci 34, 1897–1903 (2013). https://doi.org/10.1007/s10072-013-1401-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10072-013-1401-1